Factors predicting male fertilization success in an external fertilizer

In postcopulatory sexual selection both sperm competition and cryptic female choice are considered to be important selective agents, but their relative importance for male fertilization success has received little attention. We tested whether sperm quality, male spawning coloration, male heterozygosity, and genetic overlap with the female explained a male’s fertilization success in controlled in vitro fertilization competition trials between equal numbers of sperm from pairs of male Arctic charr (Salvelinus alpinus), an external fertilizer. Offspring were genotyped to determine each males’ share of paternity. The velocity of a male’s sperm relative to the velocity of the competing male’s sperm was the best predictor of male fertilization success. Yet, sperm velocity was not related to spawning coloration or male heterozygosity. In fact, the most brightly colored male in a pair had the lowest fertilization probability. This could result from cryptic female choice for pale males, but might rather be a result of paler males producing more competitive sperm than more colored males. Furthermore, the more microsatellite alleles a male shared with the female relative to the competing male, the higher fertilization success he had. We argue that this latter may be an effect of assortative cryptic female choice, which might prevent hybridization with sympatric Arctic charr morphs or one form of kin selection.     

The effects of male and female genotype on variance in male fertilization success in the red flour beetle (<Emphasis Type="Italic">Tribolium castaneum</Emphasis>)

The number of eggs fertilized by a male at any given copulation (fertilization success) is affected by a large number of factors. Male insemination and sperm competition success and various female structures and/or processes that bias paternity in favor of some males over others (cryptic female choice) are all likely to affect fertilization success. We suggest that more comprehensive measures of male fertilization success can increase our understanding of postcopulatory sexual selection. To improve our understanding of the importance of various sources of variance in male fertilization success, we conducted a series of experiments using flour beetles. Different wild-type strains were used in reciprocal double mating experiments, against a phenotypic marker strain. We assessed the relative effects of female genotype, male genotype and mating order on independent and inclusive measures of male defense ability ( P ₁), male offense ability ( P ₂), and female remating behavior. Female genotype influenced both P ₁ and P ₂, and male genotype interacted strongly with female genotype in its effect on P ₂. We also documented an interaction between female and male genotypes in the effects of mating on female remating behavior, such that females tended to remate most rapidly when mated to males of their own genotype. It is clear from our experiments that cryptic female choice influences the pattern of fertilization success in flour beetles, and we suggest that cryptic female choice may often be an important component of postcopulatory sexual selection. Future investigations would benefit from studying the multiple components of variance in male fertilization success.     

Determinants of paternity success in the spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and female mating behaviour

In double mating experiments, we examined whether and to what extent various male and female behavioural traits influence the course of mating and fertilization success in the cellar spider. In males, we focussed on pre-copulatory behaviour and on the rhythmic twisting movements that the male performs with his pedipalps during copulation. In females, we investigated remating decisions and the effect of female termination of copulation. Second males fertilized a high proportion of the eggs (P ₂: median 89%) despite much shorter second matings, with high variation in relative paternity success. The number of pedipalp movements (PPMs) of either male was a better predictor of paternity than copulation duration. Our results suggest that in second matings, PPMs help to remove sperm from previous males, whereas in first matings a high number of PPMs enhances fertilization success, either due to numerical sperm competition or cryptic female choice. Furthermore, we found a negative male age effect on paternity in second matings, implying that age-related deterioration of spermatozoa may promote variation in fertilization success. Female receptivity decreased significantly in second matings; only 70% of the females remated. Females that accepted a second copulation were found to terminate these much earlier and with higher probability than first matings. This suggests that the intensity of conflict between the sexes is higher in second matings. Increased intensity of sexual conflict may be responsible for stronger selection on male traits, as pre-copulatory behaviour and age only affected male copulatory performance and paternity in second matings. Electronic Publication     

Male genital traits and mating interval affect male fertilization success in the water strider Gerris lacustris

Parker's seminal work brought attention to the possibility of postmating sexual selection by non-random fertilization success. Mechanisms for these processes are still only partly understood and there is clearly a need for more studies of intraspecific variation in sperm precedence. Here, we report results from an experimental study of the variation in fertilization success between males of the water strider Gerris lacustris. Genital morphology, male body size, and copulation duration were examined as possible correlates of paternity. The significance of guarding duration was also analysed. Only male genital morphology was correlated to fertilization success. This is one of the first studies showing a relationship between male genital traits and fertilization success, supporting the view that sexual selection may be responsible for the rapid and divergent evolution of genital structures in animals with internal fertilization. The fertilization success of last males varied considerably after double matings with a short mating interval (10 min). Last-male priority ranged from 0 to 100% and usually one of the males involved fertilized almost all the eggs. After double matings with a short mating interval, the proportion of eggs fertilized by the last male averaged 0.68 and was greater than 0.5. In contrast, the average fertilization success was biased towards the first male when the matings were more spread out over time (24 h). These results do not support earlier suggestions of a widespread last-male sperm priority in water striders. Received: 28 July 1998 / Received in revised form: 15 March 1999 / Accepted: 28 March 1999     

Female benefit,male risk: Polyandry in the true armyworm Pseudaletia unipuncta

In Lepidoptera polyandry is common and females may increase their lifetime reproductive output through repeated matings if they acquire essential resources from male ejaculates. However, the paternity of males mating with previously-mated females is far from assured unless sperm precedence is absolute. In this study on the polyandrous armyworm, Pseudaletia unipuncta, we used two strains of male (the black-eyed wild type and a red-eyed homozygous, recessive mutant), mated with red-eyed females, to determine (i) whether male investment has any impact on female reproductive output, and (ii) if females do benefit from multiple matings, to what extent males fertilize the eggs to which they contributed. Multiple mating resulted in a significant increase in both the fecundity and longevity of females. However, the degree of sperm precedence (those eggs fertilized by the second male) varied from 0–100%, but was not affected by either male size or age, or by the duration of copulation. In cases where sperm precedence was <50% (x = 12%) females produced significantly more eggs (1384 versus 940) prior to the second mating than females where sperm precedence was >50% (x = 89%), indicating that the quality of the first mating influenced the fertilization success of the female's second mate.     

Gene flow via the dispersal of fertilizing sperm in a colonial ascidian (Botryllus schlosseri): the effect of male density

In marine invertebrate taxa with restricted larval dispersal, the movement of fertilizing sperm may contribute significantly to gene flow. Several recent studies have examined the ability of isolated males to fertilize eggs as a function of distance, but none has explicitly considered the effect of other males in the vicinity on the spatial distribution of fertilizations obtained by a male. I assayed the effect of additional males on the fertilization success of male Botryllus schlosseri (Pallas) colonies with respect to distance via an in situ mating experiment performed in Maine, USA during the summer of 1993. Allozyme markers were used to assay paternity. The presence of additional males reduced the ability of a focal male to fertilize eggs in all distance classes. This suggests that competition for fertilizations among males will reduce gene flow via sperm dispersal and that the fertilization success of isolated males may over-estimate gene flow via sperm dispersal in many natural populations.     

Male asymmetry and postcopulatory sexual selection in the fly Dryomyza anilis

The significance of male asymmetry in postcopulatory sexual selection was studied in the fly Dryomyza anilis by examining whether male asymmetry is related to fertilization success. The traits measured were wing length, tibia length and the length of small and large claspers. The male claspers are situated at the tip of the abdomen, functional pair of claspers consists of a large and a small clasper on the same side of the body. These claspers are used to tap the female abdomen after sperm transfer, which has been shown to increase fertilization success for the mating male. Fertilization success was negatively related to the fluctuating asymmetry of wing length, suggesting either female preference for more symmetrical males or a relationship between male asymmetry and intrasexual selection which was reflected in mating performance. Fertilization success was also related to the length of small claspers, decreasing with increasing length of the claspers. In addition, males with asymmetrical small claspers enjoyed higher fertilization success than symmetrical ones. This study shows that fluctuating asymmetry in wing length is an important fitness trait in postcopulatory sexual selection. Since male tapping affects sperm distribution in the female's sperm storage organs, the higher fertilization success of males with asymmetrical small claspers could have a functional relationship with the asymmetrical position of female sperm storage organs. Received: 6 March 1997 / Accepted after revision: 8 November 1997     

Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria

Recent studies of non-random paternity have suggested that sperm selection by females may influence male fertilization success. Here we argue that the problems originally encountered in partitioning variation in non-random mating between male competition and female choice are even more pertinent to interpreting patterns of non-random paternity because of intense sperm competition between males. We describe an experiment with the yellow dung fly, Scatophaga stercoraria, designed to partition variance in the proportion of offspring sired by the second male, P ₂, between males and females, and to control for sperm competition. Large males were shown to have a higher P ₂ than small males but P ₂ was independent of the size of the female’s first mate. This result might suggest an absolute female preference for large males via sperm selection. However, large males have a higher constant rate of sperm transfer and displacement. After controlling for this effect of sperm competition, large males did not achieve higher paternity than small males. We argue that a knowledge of the mechanism of sperm competition is essential so that male effects can be controlled before conclusions are made regarding the influence of sperm selection by females in generating non-random paternity. Received: 4 April 1995 / Accepted after revision: 17 October 1995     

Sperm swimming speed and energetics vary with sperm competition risk in bluegill (<Emphasis Type="Italic">Lepomis macrochirus</Emphasis>)

Under sperm competition, a males fertilization success depends largely on the ejaculate characteristics of competing males. Theoretical models predict that, in external fertilizers, increased risk of sperm competition should result in selection for increased sperm swimming speed. To test this prediction, we studied the behavior of sperm from parental and sneaker male bluegill (Lepomis macrochirus), a fish species characterized by high levels of cuckoldry due to alternative reproductive tactics of males (parentals and cuckolders). Because cuckolders (sneakers and satellites) always spawn in the presence of a parental male, but the reverse is not true, cuckolders experience the greater risk of sperm competition. We show here that the spermatozoa of sneakers have faster initial swimming speeds but shorter periods of motility than the sperm of parental males. Moreover, we show that sperm swimming speeds shortly after activation (when most fertilization occurs) are correlated with starting ATP levels in spermatozoa, suggesting that sperm competition has selected for higher energetic capacity in the sperm of sneakers. Thus, the higher energetic capacity and initial swimming speed of sneaker sperm may explain why, despite having fewer sperm per ejaculate than parentals, sneakers fertilize more eggs than parental males when they compete to fertilize a clutch of eggs.Communicated by L.W. Simmons     

Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus

Sperm competition exerts strong selection on males to produce spermatozoa with an optimal morphology that maximizes their fertilization success. Long sperm were first suggested to be favored because they should swim faster. However, studies that investigated the relationship between sperm length and sperm competitive ability or sperm swimming velocity yielded contradictory results. More recently, ratios of the different sections of a spermatozoon (the head, midpiece, and flagellum) were suggested to be more crucial in determining swimming velocity. Additionally, sperm ability to remain and survive in the female storage organs may also influence fertilization success, so that optimal sperm morphology may rather maximize sperm longevity than velocity. In this study, we investigated how sperm morphology is related to sperm velocity and sperm longevity in the house sparrow Passer domesticus. Sperm velocity was found to be correlated with head/flagellum ratio. Sperm with small heads relative to their flagellum showed higher swimming velocity. Additionally, shorter sperm were found to live longer. Finally, we found sperm morphological traits to vary substantially within males and the head/flagellum ratio to be unrelated to total sperm length. We discuss the hypothesis that the substantial within-male variation in sperm morphology reflects a male strategy to produce a diversity of sperm from long, fast-swimming to short, long-living sperm to maximize their fertilization success in a context of sperm competition.     

No relationship between long-distance acoustic mate attraction signals and male fertility or female preference in spring field crickets

To father offspring, a male must succeed at two processes of sexual selection: (1) mate with a female and (2) fertilize her eggs. We investigated the relationships between pre- and post-copulatory male traits and female mating responses in wild-captured and laboratory-reared spring field crickets, Gryllus veletis. The phenotype-linked fertility hypothesis suggests that females may receive a direct benefit, enhanced fertilization efficiency, by mating with males that signal attractively. We measured fine-scale components of male acoustic mate attraction signals as well as how much time males spent signalling, measured female preference for males in mating trials and then quantified sperm number and viability. We found no relationship between male signalling traits and male fertility or female preference, providing no evidence for the phenotype-linked fertility hypothesis. We also found no difference in sperm metrics between wild-captured and laboratory-reared males. While female crickets may receive benefits by choosing males based on acoustic signal characteristics, whether the benefits are a result of genetic quality, seminal fluid contents or some other male trait remains unknown.     

Fertilisation success in the fly Dryomyza anilis (Dryomyzidae): effects of male size and the mating situation

Male fertilisation success in relation to male size and the mating situation (ordinary pair formation with a single, nonvirgin female vs. take overs) was examined in the fly Dryomyza anilis. In ordinary matings, large males achieved higher fertilisation success than small ones when they were the second to mate with the female. Take overs differ from ordinary pair formation in that the second male experiences intensified sperm competition. This is because in take overs the female is not able to discharge any of the sperm inseminated by the first male as she usually does before a new mating. Compared with ordinary matings, take overs reduced the fertilisation success of the second male by 8–10%, whereas that of the first male was 7–14% higher in take overs. Even though the intruder was always larger than the paired male his superior fertilisation success did not compensate for the effect of the sperm already present in the female. In D. anilis, males can increase their fertilisation success by tapping the female's external genitalia with their claspers or having several copulation bouts per mating. Thus, in a take over, the intruder could respond to the intensified sperm competition by performing more tapping sequences per copulation bout or more copulation bouts per mating. In matings observed in the wild, males performed more tapping sequences after a take over than after pair formation with a single female, although the difference was not significant. The results show that there are differences in fertilisation success between males of different size. In addition, different mating situations can result in considerable variation in the fertilisation success of an individual male. Higher fertilisation success for the first male after a take over may be significant, in particular, for the reproductive success of small males, which frequently lose their females to large males.     

Inbreeding avoidance in a poeciliid fish (Heterandria formosa)

Polyandry is hypothesized to give females an opportunity to avoid inbreeding through postcopulatory selection mechanisms if precopulatory inbreeding avoidance is not possible, for example, because of forced matings. Here, we report a postcopulatory, prefertilization, inbreeding avoidance mechanism in the least killifish, Heterandria formosa, a species in which males can force matings. Females had 50% less sperm in their oviducts and ovarian cavities after mating with a sibling compared to a mating with a nonsibling male. Neither sex showed inbreeding avoidance in a dichotomous precopulatory mate choice test or during mating trials. Females in this species invest substantially in each offspring after fertilization (matrotrophy), whereas males invest little more than sperm. Based on theory, females should therefore be more likely than males to avoid inbreeding in this species. We suggest that females do this by reducing the amount of sibling sperm in their reproductive system. However, the possibility that males invested more sperm to nonsiblings could not be ruled out. In a fertilization success experiment, the first male to mate with a female sired all the offspring in most cases, even if it was a sibling. However, large females were more likely to carry offspring of multiple males. Possibly female sperm storage sites were filled by the first male, and only large females had space for the second male's sperm.     

Age before beauty? Relationships between fertilization success and age-dependent ornaments in barn swallows

When males become more ornamented and reproduce more successfully as they grow older, phenotypic correlations between ornament exaggeration and reproductive success can be confounded with age effects in cross-sectional studies, and thus say relatively little about sexual selection on these traits. This is exemplified here in a correlative study of male fertilization success in a large colony of American barn swallows (Hirundo rustica erythrogaster). Previous studies of this species have indicated that two sexually dimorphic traits, tail length and ventral plumage coloration, are positively correlated with male fertilization success, and a mechanism of sexual selection by female choice has been invoked. However, these studies did not control for potential age-related variation in trait expression. Here, we show that male fertilization success was positively correlated with male tail length but not with plumage coloration. We also show that 1-year-old males had shorter tails and lower fertilization success than older males. This age effect accounted for much of the covariance between tail length and fertilization success. Still, there was a positive relationship between tail length and fertilization success among older males. But as this group consisted of males from different age classes, an age effect may be hidden in this relationship as well. Our data also revealed a longitudinal increase in both tail length and fertilization success for individual males. We argue that age-dependent ornament expression and reproductive performance in males complicate inferences about female preferences and sexual selection.     

Multiple paternity and individual variation in sperm precedence in the simultaneously hermaphroditic land snail Arianta arbustorum

Intraspecific variation in the proportion of offspring sired by the second mate with a female (P₂) is an aspect of sperm competition that has received little attention. I examined the effects of delay between copulations (range 9–380 days) and size of sperm donor on sperm precedence in double-mated individuals of the simultaneously hermaphroditic land snail Arianta arbustorum. Using shell colour as a genetic marker, paternity was analysed in 132 broods produced by 35 snails that had mated with two partners of different genotype. Sperm precedence (P₂) was influenced by the time between the two matings when the mating delay exceeded 70 days (one reproductive season). P2 averaged 0.34 in the first brood of snails that mated twice within 70 days indicating first mate sperm precedence. In contrast, P₂ averaged 0.76 in broods of snails that remated in the following season, indicating a decreased viability of sperm from the first mate. The size of sperm-donating individuals had no effect on the fertilization success of their sperm in the first brood produced after the second copulation. Analysis of long-term sperm utilization in 23 snails that laid three to nine egg batches over 2 years revealed striking differences among individuals. Five snails (21.7%) exhibited first-mate sperm precedence throughout, eight snails (34.8%) showed second-mate sperm precedence throughout, whereas ten snails (43.5%) exhibited sperm mixing in successive batches. It is suggested that the individual variation in sperm precedence in A. arbustorum may partly be due to differences in the amount of sperm transferred. Paternity analysis in 34 batches laid by 19 wild-caught individuals of A. arbustorum indicated that at least 12 snails (63.2%) used sperm from two or more mates for the fertilization of their eggs. This suggests a high incidence of multiple paternity in broods of A. arbustorum under field conditions.     

Sequential polyandry affords post-mating sexual selection in the mouths of cichlid females

Females mating with multiple males may obtain direct benefits such as nuptial gifts or paternal care or indirect (i.e. genetic) benefits resulting in higher-quality offspring. While direct benefits are easily identified, it is difficult to determine indirect benefits, and it is hence largely unclear how they are obtained. This is particularly true in species with external fertilisation, where females seem to have little control over fertilisation. In cichlids, most maternal mouthbrooders show sequential multiple mating, where females visit several males for egg deposition. Genetic data revealed that multiple paternity of eggs and young in the mouth of females is common, but behavioural data of female spawning decisions are missing. Here, we test four hypotheses to explain female multiple mating in the maternally mouthbrooding cichlid, Ophthalmotilapia ventralis: (1) fertilisation insurance, (2) genetic bet-hedging, (3) female choice and (4) ‘sperm shopping’ (i.e. induction of sperm competition resulting in sexually selected sperm). Detailed observations of spawning behaviour in the field combined with histological analyses of the male reproductive organs suggest that fertilisation insurance, genetic bet-hedging and pre-mating female choice are unlikely to explain the sequential female multiple mating in O. ventralis. Instead, cryptic female choice by sperm shopping, i.e. post-mating sexual selection, is most compatible with our data and might be the major ultimate cause of multiple mating in females of this species and of mouthbrooding cichlids with maternal care in general. Our study provides new insight into ultimate causes of sequential polyandry in species with external fertilisation, as hitherto post-mating sexual selection by cryptic female choice has been assumed to be incompatible with external fertilisation mechanisms except by components of the ovarian fluid.     

Sperm competition and evidence of sperm fertilization patterns in the carrion ball-roller beetle Canthon cyanellus cyanellus LeConte (Scarabaeidae: Scarabaeinae)

Field observation and laboratory experiments were conducted to investigate sperm competition and patterns of sperm fertilization under different experimental conditions in the carrion ball-roller beetle Canthon cyanellus cyanellus. Males in nature can mate with females whose spermathecae contains fertile sperm from other males. Sperm precedence was investigated using a visible genetic marker. The progeny of red (homozygous recessive) virgin females mated once with a red male and afterward, once with a green beetle (homozygous dominant) and vice versa, revealed that regardless of its color, the last male to mate fertilized c.a. 50% of the eggs, suggesting strong sperm competition. Males were able to achieve higher levels of paternity (more than 80%) when mated ad libitum with previously mated females, although large amount of variance in paternity does not exclude the possibility of first male sperm precedence or female cryptic choice. These results suggest that repeated mating and sperm replacement are the mechanisms by which last males achieve sperm precedence.     

Female control of extra-pair fertilization in tree swallows

Summary In a Canadian population of tree swallows, Tachycineta bicolor, DNA fingerprinting has previously shown that half of all broods contain many offspring resulting from extra-pair copulations (EPCs), whereas the other half contain only legitimate offspring. This bimodal pattern of extra-pair paternity might be due to variation in the effectiveness of male paternity guards, variation in female ability to resist EPCs, and/or variation in female pursuit of EPCs. Here we report experimental evidence for female control of copulations and fertilizations and the occurrence of two alternative copulation strategies among females in this population. Ten paired male tree swallows were removed on the day their mates laid the first egg. Replacement males took over the nestbox within 0.5–23 h and attempted to copulate with the widowed female. Assuming that eggs were fertilized approximately 24 h prior to laying, the first two eggs were fertilized before the male was removed, while the third and subsequent eggs could potentially be fertilized by the replacement male. Fingerprinting revealed that the first two eggs were sired by the resident males in five nests and by extra-pair males in the remaining five nests. The widows that had been faithful to their initially chosen mate rejected copulation attempts by the replacement male until most of the eggs had been laid. Consequently, nearly all eggs laid by these females were sired by the original male. The widows that had been unfaithful prior to male removal copulated sooner with the replacement male than females that were faithful to their mate. However, these replacement males also had a very low fertilization success; most eggs were sired by males that were not associated with the nest. This is consistent with the situation in non-experimental nests where unfaithful females copulate with their mate at the same rate as faithful females, yet unfaithful females have a majority of offspring sired by extra-pair males. We conclude that fertilization patterns to a large extent are determined by the female through active selection and rejection of copulation partners, though our results also allow some speculation that females have control over sperm competition. Female copulation tactics are probably determined some currently unknown fitness benefits of having the offspring sired by particular males.Correspondence to: Raleigh J. Robertson     

Variations in sperm motility of the Atlantic herring Clupea harengus

Sperm characteristics and fertilization success were measured in two groups of Manx autumn-spawning herring, Clupea harengus L., captured 1 wk apart. Samples contained motile sperm for up to 45 min after activation (average 7 min). Individual spermatozoa were motile for up to 5 min. The activation of individual spermatozoa is probably phased, although the mechanism for the delay is not clear. This can account for the overall low levels of active sperm at any one time, the periodic fluctuations observed in the proportion of motile sperm, and for successful fertilization rates achieved using samples of apparently immotile sperm. The proportion of motile sperm was not affected by the presence of eggs, but the duration of motility was longer when sperm was activated in the presence of eggs rather than in seawater alone. Individual males differed significantly in the duration of motility in their sperm samples and in the fertilization rates achieved, but not in the proportion of motile sperm in each sample. There were no consistent changes in the characteristics of the spawners or the sperm between the two sample dates. Sperm motility and duration of motility were significantly correlated, but none of the sperm characteristics measured was significantly related to fertilization success. Received: 13 March 1999 / Accepted: 20 May 1999     

Mating patterns and a test for female mate choice in Etheostoma spectabile (Pisces,Percidae)

Neither size nor breeding color correlated with spawning success of male orangethroat darters, Etheostoma spectabile (Pisces, Percidae), under natural field conditions. When females were presented experimentally with a simultaneous choice they spent no more time in proximity to large than small males, and were subsequently no more likely to spawn with large than with small males. Females also displayed no preference for bright versus dull males. Males and females did not differ significantly in size. Etheostoma spectabile may lack sexual size dimorphism as a result of the lack of female choice for size and the ineffectiveness of male attempts to monopolize females, or selection may be for increased size of females. Males are not dwarfs because of sperm competition. Contest competition among males appeared to be important in initiating spawnings but many males obtained spawnings by participating in ongoing spawning events. Etheostoma spectabile is an example of a sexually dimorphic species with no evident female preference for male size or color.